The gateway to Africa: What determines sea crossing performance of a migratory soaring bird at the Strait of Gibraltar?

Large bodies of water represent major obstacles for the migration of soaring birds because thermal updrafts are absent or weak over water. Soaring birds are known to time their water crossings with favourable weather conditions and there are records of birds falling into the water and drowning in large numbers. However, it is still unclear how environmental factors, individual traits and trajectory choices affect their water crossing performance, this being important to understand the fitness consequences of water barriers for this group of birds. We addressed this problem using the black kite Milvus migrans as model species at a major migration bottleneck, the Strait of Gibraltar. We recorded high-resolution GPS and triaxial accelerometer data for 73 birds while crossing the Strait of Gibraltar, allowing the determination of sea crossing duration, length, altitude, speed and tortuosity, the flapping behaviour of birds and their failed crossing attempts. These parameters were modelled against wind speed and direction, time of the day, solar irradiance (proxy of thermal uplift), starting altitude and distance to Morocco, and age and sex of birds. We found that sea crossing performance of black kites is driven by their age, the wind conditions, the starting altitude and distance to Morocco. Young birds made longer sea crossings and reached lower altitude above the sea than adults. Crosswinds promoted longer sea crossings, with birds reaching lower altitudes and with higher flapping effort. Birds starting at lower altitudes were more likely to quit or made higher flapping effort to complete the crossing. The location where birds started the sea crossings impacted crossing distance and duration. We present evidence that explains why migrating soaring birds accumulate at sea passages during adverse weather conditions. Strong crosswinds during sea crossings force birds to extended flap-powered flight at low altitude, which may increase their chances of falling in the water. We also showed that juvenile birds assume more risks than adults. Finally, the way in which birds start the sea crossing is crucial for their success, particularly the starting altitude, which dictates how far birds can reach with reduced flapping effort.

Wind turbines cause functional habitat loss for migratory soaring birds.

Wind energy production has expanded to meet climate change mitigation goals, but negative impacts of wind turbines have been reported on wildlife. Soaring birds are among the most affected groups with alarming fatality rates by collision with wind turbines and an escalating occupation of their migratory corridors. These birds have been described as changing their flight trajectories to avoid wind turbines, but this behaviour may lead to functional habitat loss, as suitable soaring areas in the proximity of wind turbines will likely be underused. We modelled the displacement effect of wind turbines on black kites (Milvus migrans) tracked by GPS. We also evaluated the impact of this effect at the scale of the landscape by estimating how much suitable soaring area was lost to wind turbines. We used state-of-the-art tracking devices to monitor the movements of 130 black kites in an area populated by wind turbines, at the migratory bottleneck of the Strait of Gibraltar. Landscape use by birds was mapped from GPS data using dynamic Brownian bridge movement models, and generalized additive mixed modelling was used to estimate the effect of wind turbine proximity on bird use while accounting for orographic and thermal uplift availability. We found that areas up to approximately 674 m away from the turbines were less used than expected given their uplift potential. Within that distance threshold, bird use decreased with the proximity to wind turbines. We estimated that the footprint of wind turbines affected 3%-14% of the areas suitable for soaring in our study area. We present evidence that the impacts of wind energy industry on soaring birds are greater than previously acknowledged. In addition to the commonly reported fatalities, the avoidance of turbines by soaring birds causes habitat losses in their movement corridors. Authorities should recognize this further impact of wind energy production and establish new regulations that protect soaring habitat. We also showed that soaring habitat for birds can be modelled at a fine scale using publicly available data. Such an approach can be used to plan low-impact placement of turbines in new wind energy developments.

Co-Occurrence of Francisella, Spotted Fever Group Rickettsia, and Midichloria in Avian-Associated Hyalomma rufipes.

The migratory behavior of wild birds contributes to the geographical spread of ticks and their microorganisms. In this study, we aimed to investigate the dispersal and co-occurrence of Francisella and spotted fever group Rickettsia (SFGR) in ticks infesting birds migrating northward in the African-Western Palaearctic region (AWPR). Birds were trapped with mist nests across the Mediterranean basin during the 2014 and 2015 spring migration. In total, 575 ticks were collected from 244 birds. We screened the ticks for the species Francisella tularensis, the genus Francisella, and SFGR by microfluidic real-time PCR. Confirmatory analyses and metagenomic sequencing were performed on tick samples that putatively tested positive for F. tularensis during initial screenings. Hyalomma rufipes was the most common tick species and had a high prevalence of Francisella, including co-occurrence of Francisella and SFGR. Metagenomic analysis of total DNA extracted from two H. rufipes confirmed the presence of Francisella, Rickettsia, and Midichloria. Average nucleotide identity and phylogenetic inference indicated the highest identity of the metagenome-assembled genomes to a Francisella-like endosymbiont (FLE), Rickettsia aeschlimannii, and Midichloria mitochondrii. The results of this study suggest that (i) FLE- and SFGR-containing ticks are dispersed by northbound migratory birds in the AWPR, (ii) H. rufipes likely is not involved in transmission of F. tularensis in the AWPR, and (iii) a dual endosymbiosis of FLEs and Midichloria may support some of the nutritional requirements of H. rufipes.

Black kites of different age and sex show similar avoidance responses to wind turbines during migration.

Populations of soaring birds are often impacted by wind-power generation. Sex and age bias in turbine collisions can exacerbate these impacts through demographic changes that can lead to population decline or collapse. While several studies have reported sex and age differences in the number of soaring birds killed by turbines, it remains unclear if they result from different abundances or group-specific turbine avoidance behaviours, the latter having severer consequences. We investigated sex and age effects on turbine avoidance behaviour of black kites (Milvus migrans) during migration near the Strait of Gibraltar. We tracked the movements of 135 individuals with GPS data loggers in an area with high density of turbines and then modelled the effect of proximity of turbines on bird utilization distribution (UD). Both sexes and age classes showed similar patterns of displacement, with reduced UD values in the proximity of turbines and a clear peak at 700-850 m away, probably marking the distance at which most birds turn direction to avoid approaching the turbines further. The consistency of these patterns indicates that displacement range can be used as an accurate proxy for collision risk and habitat loss, and should be incorporated in environmental impact assessment studies.

Association between guilds of birds in the African-Western Palaearctic region and the tick species Hyalomma rufipes, one of the main vectors of Crimean-Congo hemorrhagic fever virus.

INTRODUCTION: The ecology of the vertebrate host contributes to the geographical range expansion of ticks. In this study, we investigated which tick taxa that infest and are dispersed by birds along African-Western Palaearctic flyways during northward migration, and whether bird ecology was associated with tick taxa. MATERIALS AND METHODS: Ticks were collected from birds trapped at bird observatories in Spain, Italy, Greece, and Israel during the spring migration of 2014 and 2015, using mist nets. The tick-infested bird species were classified into guilds, using different combinations of the variables: migration distance, wintering region, foraging behaviour, and winter habitat. Ticks were molecularly determined to genus and species level by sequencing fragments of the 12S ribosomal DNA (rDNA) gene and by phylogenetic inference, using the Maximum Likelihood algorithm. Data were analysed using descriptive measures, graphs, Chi2 tests, the Tukey-Kramer test, and a parametric linear model (generalized linear model) in order to analyse and adjust for characteristics in the bird guilds and their relationship to collected tick taxa. RESULTS: Most (84.2%) of the 10,209 trapped birds were long-distance migrants, of which 2.4% were infested by ticks. The most common tick species was Hyalomma rufipes (77.7%; 447/575), a known vector and reservoir of Crimean-Congo hemorrhagic fever virus. Bird guilds containing only long-distance migrants with wintering areas in Africa were associated with the tick species H. rufipes (p < 0.0001). Furthermore, bird winter habitat was associated with H. rufipes (p = 0.003); with bird species overwintering in open habitat (p = 0.014) and wetlands (p = 0.046) having significantly more H. rufipes as compared to birds with a winter habitat comprising forest and shrubs (p = 0.82). CONCLUSIONS: With climate change, the likelihood of establishment of permanent Hyalomma populations in central and northern Europe is increasing. Thus, surveillance programs for monitoring the risk of introduction and establishment of H. rufipes in the Western-Palaearctic should be established. Our study suggests that migratory bird species wintering in African open habitats and wetlands are good candidates for monitoring potential introduction.

Citizen science for predicting spatio-temporal patterns in seabird abundance during migration.

Pelagic seabirds are elusive species which are difficult to observe, thus determining their spatial distribution during the migration period is a difficult task. Here we undertook the first long-term study on the distribution of migrating shearwaters from data gathered within the framework of citizen science projects. Specifically, we collected daily abundance (only abundance given presence) of Balearic shearwaters from 2005 to 2017 from the online databases Trektellen and eBird. We applied machine-learning techniques, specifically Random Forest regression models, to predict shearwater abundance during migration using 15 environmental predictors. We built separated models for pre-breeding and post-breeding migration. When evaluated for the total data sample, the models explained more than 52% of the variation in shearwater abundance. The models also showed good ability to predict shearwater distributions for both migration periods (correlation between observed and predicted abundance was about 70%). However, relative variable importance and variation among the models built with different training data subsamples differed between migration periods. Our results showed that data gathered in citizen science initiatives together with recently available high-resolution satellite imagery, can be successfully applied to describe the migratory spatio-temporal patterns of seabird species accurately. We show that a predictive modelling approach may offer a powerful and cost-effective tool for the long-term monitoring of the migratory patterns in sensitive marine species, as well as to identify at sea areas relevant for their protection. Modelling approaches can also be essential tools to detect the impacts of climate and other global changes in this and other species within the range of the training data.

Desert crossing strategies of migrant songbirds vary between and within species.

Each year, billions of songbirds cross large ecological barriers during their migration. Understanding how they perform this incredible task is crucial to predict how global change may threaten the safety of such journeys. Earlier studies based on radar suggested that most songbirds cross deserts in intermittent flights at high altitude, stopping in the desert during the day, while recent tracking with light loggers suggested diurnal prolongation of nocturnal flights and common non-stop flights for some species. We analyzed light intensity and temperature data obtained from geolocation loggers deployed on 130 individuals of ten migratory songbird species, and show that a large variety of strategies for crossing deserts exists between, but also sometimes within species. Diurnal stopover in the desert is a common strategy in autumn, while most species prolonged some nocturnal flights into the day. Non-stop flights over the desert occurred more frequently in spring than in autumn, and more frequently in foliage gleaners. Temperature recordings suggest that songbirds crossed deserts with flight bouts performed at various altitudes according to species and season, along a gradient ranging from low above ground in autumn to probably >2000 m above ground level, and possibly at higher altitude in spring. High-altitude flights are therefore not the general rule for crossing deserts in migrant songbirds. We conclude that a diversity of migration strategies exists for desert crossing among songbirds, with variations between but also within species.

Match between soaring modes of black kites and the fine-scale distribution of updrafts.

Understanding how soaring birds use updrafts at small spatial scales is important to identify ecological constraints of movement, and may help to prevent conflicts between wind-energy development and the conservation of wildlife. We combined high-frequency GPS animal tracking and fine-spatial-scale uplift modelling to establish a link between flight behaviour of soaring birds and the distribution of updrafts. We caught 21 black kites (Milvus migrans) and GPS-tracked them while flying over the Tarifa region, on the Spanish side of the Strait of Gibraltar. This region has a diverse topography and land cover, favouring a heterogeneous updraft spatial distribution. Bird tracks were segmented and classified into flight modes from motion parameters. Thermal and orographic uplift velocities were modelled from publically available remote-sensing and meteorological data. We found that birds perform circular soaring in areas of higher predicted thermal uplift and linear soaring in areas of higher predicted orographic uplift velocity. We show that updraft maps produced from publically available data can be used to predict where soaring birds will concentrate their flight paths and how they will behave in flight. We recommend the use of this methodological approach to improve environmental impact assessments of new wind-energy installations.

Molecular characterization of haemosporidian parasites from kites of the genus Milvus (Aves: Accipitridae).

Despite the ecological significance and appeal of birds of prey, many aspects of their biology remain poorly known, including the diversity of parasites infecting them in the wild. We studied the diversity and prevalence of haemosporidian parasites infecting the two species of kites of the genus Milvus, aiming to describe the phylogenetic relationships among them and with other haemosporidians, as well as their distribution in the two host species. Black kites, Milvus migrans, harboured a more diverse community of parasites, including three haplotypes of each of the three genera Plasmodium, Haemoproteus and Leucocytozoon, which also occurred at a higher prevalence than in red kites. In red kites, Milvus milvus only three haplotypes of Leucocytozoon were found. Kite parasites were not closely related to one another nor were they kite-specific: their diversity spanned various branches of the haemosporidian phylogenetic tree, and their closest relatives were found in other species (including various avian orders), although some Leucocytozoon and Haemoproteus haplotypes clustered within apparently raptor-specific parasite clades. Remarkably, Plasmodium spp. and Haemoproteus spp. infected adult black kites only, an observation which supports the hypothesis that they are transmitted at the African wintering grounds, while Leucocytozoon spp. is putatively transmitted only in Europe. Intercontinental migration of the black kite might explain the divergence of parasite diversity between these two sister species.